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PerspectivesinPlantEcology,EvolutionandSystematics23(2016)11–17
ContentslistsavailableatScienceDirect
Perspectives in Plant Ecology, Evolution and Systematics
jou rn a lh om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / p p e e s
Review
Decoding neighbour volatiles in preparation for future competition and implications for tritrophic interactions
VelemirNinkovica,∗,DimitrijeMarkovica,b,IrisDahlina
aDepartmentofCropProductionEcology,SwedishUniversityofAgriculturalSciences,Uppsala,Sweden bFacultyofAgriculture,UniversityofBanjaLuka,BanjaLuka,BosniaandHerzegovina
article info
Articlehistory:
Received14November2015 Receivedinrevisedform 13September2016 Accepted21September2016 Availableonline23September2016
Keywords:
Plant–plantcommunication Intraspecificandinterspecificcoexistence Plantadaptation
Plant–insectinteractions Naturalenemies Associationalresistance
abstract
Plantvolatilesignalscanprovideimportantinformationaboutthephysiologicalstatusandgenetic iden-tityoftheemitter,andnearbyplantscanusethisinformationtodetectcompetitiveneighbours.The noveltyofthesesignalsisthatplantseavesdroppingtovolatilesofundamagedneighboursrespondwith typicalcompetitionresponses,evenbeforecompetitiontakesplace,initiatingspecificgrowthresponses thatcanincreasetheircompetitivecapacity.Thispreparingforfuturecompetitionmechanismaffectsthe behaviourandabundanceofherbivorepestsandtheirnaturalenemies.Previously,suchresponseswere onlyknowntooccurinresponsetovolatilesreleasedbydamagedplants.However,volatileinteractions occuronlyinspecificcombinationofspecies/genotypes,indicatingthatplantsusevolatilesignalsinthe detectionandadaptiononlytosubstantialcompetitiveneighbours.
©2016TheAuthor(s).PublishedbyElsevierGmbH.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents
1. Plantvolatilesignals....................................................................................................................................11 2. Volatilesassignalsindetectionofcompetitiveneighbours...........................................................................................12 3. VOCsinducedresponsesandtritrophicinteractions ................................................................................................... 12 4. Herbivorepredatorresponsestovolatileinteractionsbetweenundamagedplants..................................................................14 5. Plantvolatilescarryinformationaboutupcomingthreats.............................................................................................14 6. Herbivorepredatorresponsestovolatileinteractionsbetweendamagedplants.....................................................................15 7. Conclusionsandfutureprospects......................................................................................................................15 Authorcontributions.....................................................................................................................................15 Acknowledgements ..................................................................................................................................... 16 References..............................................................................................................................................16 1. Plantvolatilesignals
Fromitsfirstmoment,agrowingplantisexposedtovarious challengesaffectingitssurvivalandtheplantcanrespondtothis indifferentways.Growthconditionatthesitesetsaframefor plantresourcestorespondtothesechanges.Byspendinga life-timerootedtothesameplace,asaconsequenceoftheirspecific nature,neighbouringplantsconstantlysharethesameavailable resources.Thus,coexistencewithotherplantsispermanentandthe
∗ Correspondingauthorat:DepartmentofCropProductionEcology,Swedish Uni-versityofAgriculturalSciences,Box7043,SE-75007Uppsala,Sweden.
E-mailaddress:velemir.ninkovic@slu.se(V.Ninkovic).
mostimportantchallengethatindividualplantsfaceduringtheir lifecycle.Inordertoprepareforcompetitionwithnearbyplants andpossibleupcomingthreats,plantsmonitoranddetectreliable signals,towhichtheyrespondwithgreatsensitivityand discrimi-nation(BallarèandCasal,2000;Clarketal.,2001;Trewavas,2005).
Inorderforaplanttosurvive,itmustdetectthepresenceof competingindividuals,bothofthesamespecies(conspecific)and differentspecies(heterospecific),andthenadaptappropriately (HutchingsandDekroon,1994;CallawayandAschehoug,2000;
Fridleyetal.,2007;MurphyandDudley,2009;Rubertietal.,2012).
Theconsequentsignallingthatplantsperceiveforcesthemto dis-tinguishbetweencrucialsignalspredictingcompetitiveneighbours frominsignificantonesnotcrucialfortheirownfitness.Plants
http://dx.doi.org/10.1016/j.ppees.2016.09.005
1433-8319/©2016TheAuthor(s).PublishedbyElsevierGmbH.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).
12 V.Ninkovicetal./PerspectivesinPlantEcology,EvolutionandSystematics23(2016)11–17
respondtocompetitorsthroughphysiologicalandmorphological changesthatincreasetheirfitness(Callawayetal.,2003;Crutsinger etal.,2006;Violleetal.,2009).Theyhavedevelopedstrategies suchascompetition,confrontationandtolerance(Novoplansky, 2009)tooutgrow(Franklin,2008),suppress(Inderjitetal.,2011)or tolerate(ValladaresandNiinemets,2008)proximateneighbours.
Plantsdetectneighbouringplantsthroughdifferentkindsof sig-nals,suchasqualityoflight(Izaguirreetal.,2006;Franklin,2008;
Keuskampetal.,2010),acoustic(Gaglianoetal.,2012;Appeland Cocroft,2014),rootexudates(Biedrzyckietal.,2010),rootemitted volatileorganiccompounds(Deloryetal.,2016),airbornevolatile organiccompounds(Ninkovicetal.,2013),floralvolatiles(Caruso andParachnowitsch,2016)andtouch(Braam,2005;Markovicetal., 2014).Amongthecrucialsignalsareairbornevolatilesignals,which areconstantlyreleasedbyplantsintotheirsurroundings.The adap-tivestrategyoftheplantsexposedtovolatilesdependsstrongly ontheemitter’sidentity(Ninkovic,2003;Kellneretal.,2010)and itsphysiologicalstatus(Braam,2005).Physiologicalchangesin plantsrespondingtovolatilesignalscancausechanges,suchas differentvolatileprofiles,whichcanthenbeperceivedbyother plantsandorganisms(Ninkovicetal.,2013;Dahlinetal.,2015).
Thispaperaimstoreviewthepresentknowledgeonairborne volatile-mediatedinteractionsbetweenplantsandtheimplications oftheseinteractionsondifferenttrophiclevels.Wealsoidentify someresearchareasthatcallforincreasedattention.
2.Volatilesassignalsindetectionofcompetitive neighbours
Volatileorganiccompounds(VOCs)canofferimportant infor-mativevalueaboutthephysiologicalstageofeachindividualin plantcommunities.TheproductionandemissionofVOCsis devel-opmentallyregulated,increasingduringtheearlystagesofthe developmentwhenleavesareyounganddecreasingaftermaturity (Dudarevaetal.,2000).Thewayinwhichplantsrespondtothese volatilestimulidependsheavilyonthesignificanceofperceived informationandneighbouridentity,whichcanbehighlyrelatedto theageofthereceiver.Thus,youngerplantsaremoreresponsiveto futurecompetitionthanolderones(Novoplanskyetal.,1990).Since theemitterplantreleasesvolatilesignalsconstantlyinits environ-ment,itcanbeexploitedbynearbyplantsasacueforcompetitive neighbours,therebyinitiatinggrowthresponsesthatincreasethe competitivepowerofeavesdroppingplants(Dickeetal.,2003;Heil andKarban,2010).Thegeneticidentityofneighbourscanhavea significantimpactonthereceiver’sgrowthanddevelopment,since theplantssharethesameavailableresourcesbutmayhave differ-entneeds.Thecapacityofanindividualplanttorecognisenearby kinorstrangersandresponddifferentlytotheirpresence repre-sentsanimportanttraitthathelpsplantsadjusttheircompetitive abilitytoaspecificneighbour(Fridleyetal.,2007;Murphyand Dudley,2009).
Volatileemissionsfromundamagedneighbouringplantscan beimportantsignalsintheprocessofplantadaptiontothe pres-enceofpotentialcompetitors.Forexample,Ninkovic(2003)tested twobarleyvarietiesthatwereexposedtoeachotherin labo-ratoryexperimentswhereallothertypesofinteractionswere preventedexceptviavolatiles.PlantsofthebarleyvarietyKara thathadpreviouslybeenexposedtoVOCsofvarietyAlva allo-catedmorebiomasstotheirrootsthanunexposedplantsorKara exposedtoVOCsofotherKaraplants.Anincreasedrootbiomassin youngreceiverplantsmaycontributetotheirfitnessbyboosting theircapacityforbelow-groundcompetitionthroughroot prolif-erationintonutrient-richpatches.Adecreasedred:far-redlight actastheearliestneighbour-detectionsignalincompetitionfor light(e.g.,DickeandBaldwin,2010;PierikanddeWit,2014)which
induceselongationandaffectstheVOCs’emissionrateofexposed plants(Keggeetal.,2013).Inanotherexperiment,theemitting Alvaplantsgrowninlowred:far-redconditionsshowedtypical shadeavoidance,increasinginbiomassallocationtoshootsand changingemissionoftheirvolatileblend(Keggeetal.,2015).Such alteredvolatileemissionofAlvainducedatypicalshadeavoidance responseofexposedKaraplantsthataccumulatedmoreresources intoshoot-andleaf-biomassthantoroots.Theseexamplesshow thatVOCsactsasdetectingsignalsthathaveimportant informa-tivevalueaboutthephysiologicalstatusofneighbouringplants, whichcaninduceresponsesinreceivingplantstopreparefor futurecompetition.Theextraordinarynoveltyofplants’ability tousevolatilecuestopredicttheexistenceofforthcoming com-petitiveneighboursisreflectedintheresponsethatoccurseven beforecompetitiontakesplace.Thispreparingforfuture compe-titionmechanismalsooperatesbetweenundamagedneighbours ofdifferentspecies:potatoplantsthatwerepreviouslyexposedto volatilesfromonionplantschangedtheirvolatileprofileby releas-ingconsiderablygreaterquantitiesoftwoterpenoids(Ninkovic etal.,2013).Suchresponseswerepreviouslyonlyknowntooccur inresponsetovolatilesreleasedbydamagedplants(Dickeand Baldwin,2010;Karbanetal.,2014).Thus,VOCscarryinformation aboutwhetherneighbouringplantsareunderattack,butalsoabout theemitterplantsthemselves,whichenablesthemtomakespecific preparationsforfuturecompetition.
TheaboveexamplesshowthatVOCs(a)actasneighbour detec-tionsignals,(b)mediateinter-andintraspecificplantinteractions, (c)haveimportantinformativevalueaboutneighbouringplants, and(d)induceresponsesinreceivingplantsthatprepareforfuture competition.However,thereisaneedforfurtherstudiestoprovide knowledgeabouttheunderlyingmechanismsthatareresponsible forplants’abilitytoadapttocompetitiveneighboursby respond-ingtotheirvolatiles.Interactionsbetweenplantsareverycomplex andmayhavesignificantecologicalimplications.Thefactthatthe behaviourofinsectscanbeaffectedgivesthisphenomenoneven widerecologicalsignificance.
3. VOCsinducedresponsesandtritrophicinteractions
Volatile interactions between undamaged plants induce changesinreceivingplantswiththepotentialtoinfluence organ-ismsathighertrophiclevels(Fig.1AandTable1)(Glinwoodetal., 2011;Ninkovicetal.,2013).Theterm‘allelobiosis’hasbeen intro-ducedtodescribethisprocessanditseffectsonreceivingplants andathighertrophiclevels(Petterssonetal.,2003;Ninkovicetal., 2006).Innaturalhabitats,theleavesofbirchBetulaspp.adsorband thenre-releasespecificherbivorerepellingvolatilesproducedby RhododendrontomentosumHarmaja,reducingtheirattractiveness toherbivorousinsects(Himanenetal.,2010).Broccolialsoshowed thesameabilitytoadsorbandre-releaseR.tomentosumvolatiles, becominglesssusceptibletoPlutellaxylostella(L.)ovipositionand lessfavouredanddamagedbytheirlarvae(Himanenetal.,2015).
Thechangedvolatileemissionofonion-exposedpotatoplantsin theabovementionedexampleresultedintheavoidanceofboth wingedandwinglessMyzuspersicae(Sulzer)morphs(Ninkovic etal.,2013;Dahlinetal.,2015),indicatingthatactiveresponseto volatilesfromneighbouringplantsmayevenhaveeffectson her-bivorousinsects.However,thisonlyoccursinspecificcombinations ofplantspecies.Thus,volatilechemicalinteractionsbetween dif-ferentweedspeciesandbarleyonlyaffectedaphidplantacceptance afterexposureoftwoweedspecies,indicatingthatthesetypesof interactionsaredependentontheplantspeciesinvolved(Glinwood etal.,2004;Ninkovicetal.,2009;DahlinandNinkovic,2013).
Ithasbeenhypothesisedthatdiversifiedcropscauseareduction intheabundanceofherbivorousinsects(NorrisandKogan,2005).
V.Ninkovicetal./PerspectivesinPlantEcology,EvolutionandSystematics23(2016)11–17 13
Fig.1.Volatilesreleasedfromnearbyundamaged(A)heterospecificand(B)conspecificcompetitorinduceadaptiveresponsesinreceivingplantwithfurtherimplicationson othertrophiclevels.(C)Changedvolatileemissionafterdamage(herbivoreormechanicalforce)ofheterospecificor(D)conspecificcompetitorsinduceadaptiveresponses inreceivingplantswithfurtherimplicationsonothertrophiclevels.
However,somestudieshaveindicatedthatdiversificationhadno effect,orincreasedherbivoredensities.Inareviewof150 stud-iesontheeffectsofdiverseagroecosystemsoninsectherbivores, Risch,AndowandAltieri(Rischetal.,1983)foundthat53percent oftheherbivorespecieswerelessabundantindiversesystems, 18percentincreased,20percentshowedavariedresponseand 8percentdidnotdifferbetweenthesystems.Thevariableeffect ofincreasedbotanicaldiversityontheoccurrenceofherbivores couldbeduetodifferencesintheadaptabilityofplantstorespond toneighbours.Thefactthatnotallplantsrespondedtovolatile sig-nalsfromtheirspecificneighbourssuggeststhatplantsmaynot respondtoinsignificantsignalsormaynotconsidertheir neigh-boursaspotentialcompetitors.Thus,theabilityofplantstoadapt toaspecificneighbourisdynamic,whichcanhavedifferent out-comesonspecificplant–insectinteractions(DahlinandNinkovic, 2013).Neighbouringplantsthatarenotconsideredcompetitors stillmayhaveabeneficialroletofocalplantsduetotheprocesses ofassociationalresistance(Barbosaetal.,2009)whichmaymake plantslessexposedtopestattack(Marquisetal.,2002;Himanen etal.,2015).
However,VOCshavebeenshowntoeveninduceresponsesin differentvarieties/genotypesofthesameplantspeciesthataffect plantdefenceagainstherbivores(Fig.1B).Changesinthegrowthof receiversandbiomassallocationpatternsinbarley,afterexposure toanothervariety(Ninkovic,2003),indicatethatcertain
physio-logicalchangeswithinplantscouldhavefurtherimplicationson herbivores.Petterssonetal.(1999)werethefirsttoshowthat volatilecommunicationbetweendifferentbarleyvarietiesmay reducetheacceptabilityofexposedplantsforRhopalosiphumpadi L.Certaincombinationsofbarleygenotypes,followedbyvolatile exposure,significantlyreducedaphidacceptance,bothin labora-toryandfieldexperiments(Ninkovicetal.,2002).Asaconsequence oftheselectionprocess,somebarleyvarietiesbecamegoodsignal emitterswhileothervarietiesbecamebetterreceivers.Ingeneral, olderbarleygenotypesdisplayedagreatertendencytorespond tovolatileexposure,whereasmorerecentonesaremorelikely tobeinducers(Kellneretal.,2010).Genotypesthathadshown areducedaphidacceptancealsorespondedtovolatileexposure fromaparticulardifferentgenotypewithloweraphidgrowth (NinkovicandÅhman,2009).Studieshaveshownthat interac-tionbetweenplantsindiversewheatvarietymixturesreduces R.padiperformance,affectingmotheraphidsizethatdecreased offspringproductionandloweraphidpopulation(Shoffnerand Tooker,2013;GrettenbergerandTooker,2016).Theempirical resultsofthesestudiessupportthenotionthatvolatile communi-cationrepresentsaneffectiveandrapidmeansofsignallingamong plantsprovidinginformationofthesameordifferentindividuals astheemitter.
Inplantpopulation,individualsreactdifferentlytocuesof sur-roundingplants,whichmaybenefitrespondersbyincreasingthe
14 V.Ninkovicetal./PerspectivesinPlantEcology,EvolutionandSystematics23(2016)11–17
Table1
Surveyoftheexamplesonvolatilecommunicationbetweenundamagedplantsofthesameanddifferentspecieswiththespecificeffectsontritrophicinteractionsdueto inducedresponsesofthereceivingplants.
Author(s) Emitterplant Receiver Inducedeffects
a)Betweendifferentplantspecies
Glinwoodetal.(2004) Certainweedspecies Barley Reducedaphidacceptance
Ninkovicetal.(2009) Certainweedspecies Barley Reducedaphidacceptance
DahlinandNinkovic(2013) Certainweedspecies Barley Reducedaphidpopulationdevelopment
Ninkovicetal.(2013) Onion Potato Changedvolatileprofile,reducedaphidhostplant
acceptanceandaphidimmigrationrate
Dahlinetal.(2015) Onion Potato Reducedaphidplantacceptance
Himanenetal.(2010) Rhododendrontomentosum Betulapendula Adsorptionandre-releaseofherbivorerepellingvolatiles Himanenetal.(2015) R.tomentosum Brassicaoleracea Adsorptionandre-releaseofspecificvolatiles,reduced
ovipositionandlarvalfeeding NinkovicandPettersson(2003) Couchgrass/thistle Barley Increasedattractivenessofladybirds
Vuceticetal.(2014) Onion Potato Changedolfactoryresponsesofaphids,increased
attractivenessofladybirds b)Betweenvarietiesofthesameplantspecies
Ninkovic(2003) Barley Barley Biomassallocationtoroots
Keggeetal.(2015) Barleyinreducedlight Barley Biomassallocationtoshoots
Petterssonetal.(1999) Barley Barley Reducedaphidacceptanceandgrowth
Kellneretal.(2010) Barley Barley rateincertainvarietiescombinations
NinkovicandÅhman(2009) Barley Barley
Ninkovicetal.(2002) Barley Barley Reducedaphidacceptanceincertainvarieties
combinations
ShoffnerandTooker(2013) Wheat Wheat Reducedaphidgrowthrate
GrettenbergerandTooker(2016) Wheat Wheat Reducedaphidoffspringproduction
Ninkovicetal.(2011) Barley Barley Increasedattractivenessforladybirds
inclusivefitnessofcloseneighbours.Thereisaclearbenefitinthe VOCs’detectionandresponsetothepresenceofthe“right” neigh-bour(specificgenotype),asitmayaffectinsectbehaviour.The abovementionedexamplesconfirmthebenefitforsignalreceivers andstrengthenthehypothesisthatanincreasinggenotypic diver-sityincropfieldscouldgreatlyimproveinsectpestmanagement (CanteloandSanford,1984;Power,1991;Ninkovicetal.,2002;
TookerandFrank,2012;GrettenbergerandTooker,2015). Inter-actionsbetweenplantsarecontextdependentandinfluencednot onlybyspeciesorgenotypebutalsobytheenvironmentandthe physiologicalstateoftheplants(Andow,1991;Barbosaetal.,2009;
BartonandKoricheva,2010).
4.Herbivorepredatorresponsestovolatileinteractions betweenundamagedplants
Interactionsbetweenundamagedplantspeciescanleadtothe alternationofhabitatandpreysearchingbehaviourofpredatory insects,evenwhenpreywerenotpresent(Fig.1A)(Priceetal., 1980;Bottrelletal.,1998;NinkovicandPettersson,2003;Glinwood etal.,2009;Ninkovicetal.,2011).Thus,ladybirdoccurrencewas significantlyhigherinpatchescontainingeithercouchgrass Elytri-giarepens(L.)Desv.exNevskiorthistlesCirsiumarvense(L.)Scop.
theninweedlesspatchesinabarleyfield(NinkovicandPettersson, 2003).Subsequentlaboratorystudiesshowedthatitwasnotthe VOCsoftheweedsbythemselvesthatattractedtheladybirds;
instead,ladybirdsweremoreattractedtotheVOCsofbarleyplants thatwerepreviouslyexposedtoVOCsfromC.arvensethantothat ofunexposedbarley(NinkovicandPettersson,2003).These find-ingsareinlinewithanotherstudyshowingthatladybirdswere significantlymoreattractedtoonion-exposedpotatothatresulted inanincreasedemissionoftwoterpenoidsthanunexposed pota-toes(Vuceticetal.,2014).Thesefindingssuggestthatchanged VOCsinducedbyvolatilecommunicationbetweenplantscanaffect attractionofpredators,whichcanbeanunderlyingmechanism thatcontributestoanincreasedabundanceofnaturalenemiesin botanicallydiversefields(Vuceticetal.,2014).
Effectsofvolatilecommunicationbetweengenotypesofthe sameplantspeciesonthethird trophiclevelhave alsobeen
reported(Fig.1B)(Johnson,2008;Glinwoodetal.,2009;Ninkovic etal.,2011).Significantlymoreladybirdswerefoundinplotssown withtwodifferentbarleyvarietiesthaninpureplotsofeither varietyalone(Ninkovicetal.,2011).Supportinglaboratory stud-iesshowedthatladybirdswereattractedtoVOCsofonevariety exposedtoanotherandalsotothecombinedVOCsoftwo differ-entvarieties(Glinwoodetal.,2009;Ninkovicetal.,2011).Theory suggeststhatincreasedplantspeciesdiversitycauseareduction inpestabundanceduetoanincreasednumberofnatural ene-mies(Andow,1991;Haddadetal.,2009;Randlkoferetal.,2010).
Thequestionremainsastowhetherdecreasedpestabundanceis causedbyhighernumbersoftheirnaturalenemiesorby associa-tionalresistanceofneighbouringplantsthatdecreasestheamount ofdamagetocropplants(Barbosaetal.,2009;DahlinandNinkovic, 2013).
5. Plantvolatilescarryinformationaboutupcomingthreats
Plants’volatilescan alsocarryinformation aboutpotential upcomingthreatsfromtheirsurroundingneighbours.Herbivorous insectsormechanicaldamagerapidlyinitiatetheassaultedplants tosubstantiallychangetheirvolatileprofileandrelease herbivore-inducedplantvolatiles(HIPVs)(Mithöferetal.,2005;Wasternack etal.,2006;D’Auriaetal.,2007;MummandDicke,2010)thatare nottypicalforundamagedplants(Dicke,1999;Hare,2011).These HIPVshaveimportantinformativevalueforundamaged neigh-bours(KarbanandMaron,2002;Arimuraetal.,2010),whichhelps thempredictimpendingherbivoreattackandinduceplantdefence responses,whichmakeplantslessattractiveandsuitablehosts forherbivores(Fig.1C)(HeilandKost,2006;Baldwinetal.,2006;
Karbanetal.,2010;Pearseetal.,2013).Insuchsituations, neigh-bouringunattackedplantsmayhaveahugeadvantagecompared tothesignalemitter,whichrequiresresourcesfordefencethat wouldotherwisebeusedincompetitionforabove-and below-groundresourceswithundamagedneighbours.However,HIPVs releasedfromadamagedplantalsohaveanimportant informa-tiverolefortheemitteritselfaswithin-plantsignalsthataimto informotherorgansofthesameplantaboutthethreat.The pri-maryfunctionofHIPVsreleasedaftertissuedamagesistotransmit
V.Ninkovicetal./PerspectivesinPlantEcology,EvolutionandSystematics23(2016)11–17 15
signalswithinthesameplant(HeilandTon,2008)butnottoinform neighbours.Thisisofparticularimportanceforplants,asthe vas-cularsignaltransportismuchslowerthanforvolatilesignalling (Orians,2005).
Closerelativeshavemoresimilarchemotypes,confirmingthat volatilesignalsfromclosedamagedkinprovidemorereliable informationthanthoseobtainedfromstrangers(Karbanetal., 2014).Suchindividualsofthesamechemotypeexchangesignals moreeffectivelyandweresignificantlylessherbivoredamaged thanindividualsofdifferentchemotypes.Arecentstudyshowed thattomatoplantsabsorbed(Z)-3-hexanolemittedbyherbivore attackedconspecificneighboursandconvertedto (Z)-3-hexenyl-vicianosidethatiseffectiveinsuppressinggrowthandsurvivalof cutworms(Sugimotoetal.,2014).Also,maizeplantsinfestedby Mythimnaseparata(Walker)releasedaspecificblendofvolatiles thatinducedefenceresponsesinconspecificneighbouringplants, reducinglarvaldevelopmentimmediatelyafterexposureorupto fivedayslater(Alietal.,2013).Theratiobetweenspecific com-poundsandtheirconcentrationiscrucialforreceivingplantsin preparationforupcomingthreats.WoundedPyrethrumplants, Tanacetumcinerariifolium(Trevir.)Sch.Bip.increasedtheemission ofseveralterpenoids,whichwereonlyeffectiveinthebiosynthesis ofpyrethrininneighbouringundamagedplantswhenallofthefive componentswereincludedintheblend(Uedaetal.,2012).Many oftheinducibleandhighlyreactiveHIPVswereshowntohavea limitedlife-timeintheatmosphere,rangingfromacoupleof min-utesupto24h(Yuanetal.,2009).Agreaterdegreeofresistance inreceivingplantsagainstherbivoresisrelatedtoalonger expo-sureperiodandahigheraccumulationofvolatilecompoundsfrom infestedplants(Chohetal.,2004).
Ithasbeendemonstrated that TrifoliumpratenseL.grown togetherwithconspecificssignificantlyreducedtheemissionof totalandherbivoreinducedvolatilescomparedtoT.pratensegrown togetherwithDactylusglomerataL.orgrowingalone(Kigathi et al.,2013).Sucharesponse of T.pratense tothe presence ofconspecificswasattributedtoareducedpossibilityofattack byspecialistherbivoresandminimisedeavesdropping of her-bivoreattackinformationbyneighbours(Fig.1D).Considering thefactthatdifferentplantspeciesemitspecificHIPVsblends andgrowatdifferentdistancesfromeachother,itis reason-abletostatethatthedefenceinductionin receivingplantsis highlycorrelatedtoexposuretime,emitterrelatednessandthe reactivityofreleasedHIPVswithatmosphericoxidants.Under nat-uralconditions,volatileexchangebetweenplantsofthesame species canoccurat distances upto 60cm, whilethe effec-tiveresponsedistancebetweenindividualsofdifferentspecies ismuchsmaller,at15–20cm(Karbanetal.,2006).Ithasalso beendemonstratedthatpartialdefoliationofAlnusglutinosa(L.) inducedresistancetothebeetleAgelasticaalni(L.)in neighbour-ingplantsofthesamespecies,whichdeclinedintheplantswith increaseddistancefromdefoliatedtrees(DolchandTscharntke, 2000).
Evenmechanicallydamagedplantscanreleasevolatile sig-nalsthatcarryinformationaboutupcomingthreats.Mechanically damagedsagebrush,ArtemisiatridentataNutt.inducedresistance toherbivoresinneighbouringplantsofthesameordifferent species(Karbanet al.,2000;KarbanandShiojiri, 2009). Con-specificreceiverssufferedmuchlessdamageafterexposureto mechanicallydamagedsagebrushduetoaccumulationof defence-relatedtranscripts,whichoccurinsimilarwaystothatobserved inherbivore-attackedplants(Kessleretal.,2006).Volatilesignals fromgeneticallyrelatedindividualshaveamuchstrongereffect,in termsofreducingherbivoredamagetoexposedplants,thansignals fromlesscloselyrelatedplants(Karbanetal.,2013).
Theaboveexamplesclearlyshowthatchemicalcuesfromboth undamagedanddamagedplantsinduceresponsesinundamaged
plants.Innature,mostplantshavetostrugglewithcompeting neighboursbeforetheygetdamagedbyherbivores.Therefore,it isexpectedthatplantresponsestoVOCsofundamaged competi-torscanhaveanevenwiderecologicalsignificanceasresponsesto HIPVs.
6. Herbivorepredatorresponsestovolatileinteractions betweendamagedplants
Volatilesfromdamagedplantscanalsoinduceresponsesin neighbouringplants,makingthemmoreattractivetoherbivore natural enemies(Fig.1CandD)(DickeandVanLoon, 2000;
Ninkovicetal.,2001;KesslerandBaldwin,2002;Haddadetal., 2009;DickeandBaldwin,2010;VanWijketal.,2011).Volatiles releasedfrominfestedplantsarealsoknowntoinducechanges inneighbouringplants,protectingthemindirectlybyattracting naturalenemies(Bruinetal.,1992;Ninkovicetal.,2001).Ina wind-tunnelexperiment,unattackedLimabeanplants,Phaseolus lunatusL.wereexposedtovolatilesemittedbylimabeanplantsthat wereinfestedbyspider-mitesTetranychusurticaeKoch.Afterfour tofivedays,theodourofLimaplantsexposedtoupwindofinfested plantsweremoreattractivetopredatorymitesPhytoseiulus per-similisAthias-HenriotthanunexposedLimabeans.Thepredatory mitesrespondedsimilarlytocottonplantsGossypiumhirsutumL.
treatedinthesameway(Dickeetal.,1990).
7. Conclusionsandfutureprospects
Researchonplantresponsestovolatilesignalshas demon-stratedthecapacityofplantstomodifytheirstrategiestomeet adiversityofecologicalchallenges.Experimentalevidencehas shown that volatile communicationbetween plants plays an importantroleinrespondingprocesseswhereinducedplanttraits contributetomechanismswithtritrophicimportance.Asthese changesareproperties ofindividuals,it isnecessarytoscale fromtheleveloftheindividualtothelevelofcommunitiesand ecosystemsinordertounderstandtheindirecteffectsofaplant’s adaptivecapacity.Thepresentreviewhasshownthatvolatile sig-nalsfromundamagedplantsmediatesimilareffectsontritrophic interactionsassignalsfromherbivore-attackedplants. Neverthe-less,volatilesignalsfromintactplantshaveattractedlessscientific attentionthansignalsfromdamagedplants,whichhavebeen stud-iedextensivelyduringthelastfourdecades.
Withregardtotheoperatingmechanisms,thereisstilla con-siderablelackofknowledgeandunderstandingoftheconsistency ofinduciblesystemstothedevelopmentalstageofneighbouring plants.Thereiscurrentlyinsufficientknowledgeaboutthelimitsof inducibleresponsesinrelationtonecessarycostsforsuccessfully growthandreproduction.Theroleofinducibleplantresponses andallelobioticmechanismscallsforanincreasedunderstanding ofseveralecological,biologicalandgeneticaspects.Phenotypes adaptedtoacertainplantcommunitymayexpressrather epi-geneticresponsestosurroundingsthatwouldprobablyoccurin subsequentgenerations.Recentstudieshaveshowntheabilityof plantstodifferentiatevolatilesignalsinformingthemabout pos-siblethreats.Itisstillunknownwhetherplantsrespondonlyto on-goingthreatsorwhethertheypreserveenergytoreactto sig-nalspredictingevenmoresevereforthcomingthreats.Themore signalspointtorisk,thegreaterthechanceofarealthreat.
Authorcontributions
VN,DMandIDwrotethepaperandDMconstructedanddrew figures.
16 V.Ninkovicetal./PerspectivesinPlantEcology,EvolutionandSystematics23(2016)11–17 Acknowledgements
ThisstudywasfinanciallysupportedbyTheSwedishResearch CouncilforEnvironment(FORMAS)(projectnumber2014-225), TheSwedishFarmers’FoundationforAgriculturalResearch(project numberH1333072)andTheCarlTryggersFoundationfor Scien-tificResearch(projectnumberCTSKF14:7).Theauthorsgratefully acknowledgeProfessorJanPetterssonforhisperspectiveand con-structivecommentsonthismanuscript.
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